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Outcome after endovascular stent graft repair of aortoenteric fistula: A systematic review
REVIEW ARTICLE Kenneth Ouriel, MD, Section Editor
Outcome after endovascular stent graft repair of aortoenteric fistula: A systematic review George A. Antoniou, MD,a Stylianos Koutsias, MD,a Stavros A. Antoniou,a Andreas Georgiakakis, MD,a Miltos K. Lazarides, MD, EBSQvasc,b and Athanasios D. Giannoukas, MD, MSc, PhD, EBSQvasc,a Larissa and Alexandroupolis, Greece Background: Aortoenteric fistula (AEF) is a critical clinical condition, which may present with gastrointestinal hemorrhage, with or without signs of sepsis. Conventional open surgical repair is associated with high morbidity and mortality. Endovascular stent graft repair has been attempted, but recurrent infection remains of major concern. We conducted a systematic review to assess potential factors associated with poor outcome after endovascular treatment. Methods: The English literature was searched using the MEDLINE electronic database up to April 2008. All studies reporting on the primary management of primary or secondary AEF with endovascular stent graft repair were considered. Results: Data were extracted from 33 reports that included 41 patients and were entered in the final analysis. Persistent/recurrent/new infection or recurrent hemorrhage developed in 44% of the patients, after a mean follow-up period of 13 months (range, 0.13-36). Secondary, as compared to primary, AEF had an almost threefold increased risk of persistent/recurrent infection. Evidence of sepsis preoperatively was found to be a factor indicating unfavorable outcome (P < .05). Persistent/recurrent/new infection after treatment was associated with worse 30-day and overall survival compared with those who did not develop sepsis (P < .05). Conclusion: Endovascular stent graft repair of AEF was associated with a high incidence of infection or recurrent bleeding postoperatively. Evidence of sepsis preoperatively was indicating poor outcome. ( J Vasc Surg 2009;49:782-9.)
Aortoenteric fistula (AEF), defined as an abnormal communication between the aortic and bowel lumen, is a devastating clinical condition necessitating immediate surgical intervention. It can occur either in the setting of a primary process involving the aorta and the gastrointestinal tract or, more commonly, secondary to previous aortic reconstructive surgery. The condition may manifest with gastrointestinal hemorrhage alone or in combination with signs of sepsis. Despite its rarity, represented by an incidence in the range of 0.02 and 0.07% in autopsy studies for primary AEF and of less than 1% in patients after abdominal aortic reconstruction, AEF represents a significant clinical entity associated with high morbidity and mortality.1-3 Conventional surgical repair consists of extra-anatomic bypass grafting and aortic ligation for primary AEF, or in the case of secondary AEF, graft excision accomplished with extra-anatomic bypass or in situ aortic reconstruction. From the Department of Vascular Surgery, University Hospital of Larissa, Faculty of Medicine, University of Thessaly,a and the Department of Vascular Surgery, “Democritus” University of Thrace.b Competition of interest: none. Correspondence: Athanasios D. Giannoukas, MD, MSc, PhD, Associate Professor of Vascular Surgery, University of Thessaly Medical School, Chairman, Department of Vascular Surgery, University Hospital of Larissa, 41000 Larissa, Greece (e-mail: [email protected]). 0741-5214/$36.00 Copyright © 2009 by The Society for Vascular Surgery. doi:10.1016/j.jvs.2008.08.068
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These surgical procedures undertaken in a critically ill, severely exsanguinated and septic patient are associated with high operative morbidity and mortality rates.1,4-6 In view of these observations, less invasive endovascular aortic procedures, associated with less operative trauma and stress for the patient, have opened an alternative treatment option for this devastating complication. There are several studies reporting successful management of AEF with endovascular techniques (Table I) providing encouraging results. However, skepticism exists whether endovascular management of AEF should merely be a “bridge” to open surgery or may constitute a permanent solution, because it remains of serious concern the placement of a prosthetic material in an already infected field. We therefore conducted a systematic review of the literature and analyzed the reported cases to determine the factors associated with poor outcome and persistent infection after endovascular treatment of AEF. METHODS Search strategy. An electronic literature search of public domain databases (MEDLINE) was performed using a Web-based search engine (PubMed) for articles published between January 1990 and April 2008. The literature search was confined to studies published in English. The keywords aortoenteric fistula; aorto-duodenal fistula,
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Table I. Characteristics of patients Study
Year
Age
Gender
P/S
Site
Cause of primary AEF
Cancer
Leonhardt et al Taylor et al17 Chisci et al18 Papacharalambous et al19 Barleben et al20 Deshmukh et al21 Broutzos et al22 Metz et al23 Ikeda et al24 Ting et al25
2008 2007 2007 2007 2007 2007 2007 2006 2006 2006
Verhey et al26 Shapiro et al27 Kotsis et al28 Biancari et al29 Suzuki et al30 Assink et al31 Gonzalez-Fajardo et al32
2006 2006 2006 2006 2005 2005 2005
Nishibe et al33 Mok et al34 Dieter et al35 Tomlinson et al36 Finch et al37
2004 2004 2002 2002 2002
82 69 56 70 54 46 85 31 64 87 59 66 83 53 58 71 32 75 68 71 67 64 90 71
M F M M M M M M M M M F F M M M M M M F M M M F
S S S P P S S P P P P P S S S S P S P P P S S P
AA TA AA AA AA TA AA TA TA TA TA AA AA AA AA AA TA AA TA TA TA AA AA AA
No No No No No No No No Yes No Yes Yes No No No No No No No No Yes Yes No Yes
Leobon et al38
2002
van Doorn et al39 D’Ancona et al40 Burks et al41
2002 2002 2001
Bond et al42 Chuter et al43 Grabs et al44 Kato et al45 Schlensak et al46 Deshpande et al47 Oliva et al48
2001 2000 2000 2000 2000 1999 1997
61 80 66 78 73 82 92 73 76 88 58 76 67 59 64 67 40
M M F F M M M F M M F M M M M M M
S P P P S P S S S S S S S P S S P
TA TA TA TA AA AA AA AA TA AA TA AA AA TA AA AA TA
NA NA NA AAA Traumatic aortic dissection NA NA Aortic trauma due to ingestion of foreign body Aortic wall invasion by esophageal carcinoma NR Esophageal carcinoma-chemoirradiation Eroding duodenal stent NA NA NA NA Aortic trauma due to ingestion of foreign body NA Mycotic thoracic aortic aneurysm Thoracic aortic aneurysm Esophageal carcinoma-esophagectomy NA NA Metastatic ovarian carcinoma-peri-aortic adenopathy NA Thoracic aortic aneurysm Mycotic thoracic aortic aneurysm Aortic ulcer NA AAA NA NA NA NA NA NA NA Esophageal carcinoma-radiotherapy NA NA Esophageal carcinoma-esophagectomy
16
Hemodynamic instability Yes No No No Yes No Yes Yes Yes Yes No Yes Yes Yes No No Yes Yes Yes
No No Yes No No No No No No No No No No Yes No Yes Yes
Infection
Type of stent graft
Fistula occlusion
Adjunctive procedure
Lifelong antibiotics
Yes Yes Yes Yes No No No Yes No Yes Yes No Yes No Yes No No No Yes
Thoracic endoprosthesis (TAG, Gore) Straight sent graft with 1 extension Tube graft endoprosthesis (Talent, Medtronic) Bifurcated aortoiliac stent graft (Lifepath) 2 aortic extension cuffs (Excluder, Gore) Aortic stent graft (Zenith, Cook) Bifurcated stent graft (Excluder, Gore) Thoracic aortic stent graft (TAG, Gore) Gianturco Z-stent graft (Cook) covered with a Dacron graft AneuRx Zenith Aortic cuff (AneuRx, Medtronic) Bifurcated stent graft (Excluder, Gore) Aorto-uni-iliac stent graft (Zenith, Cook), F-F bypass Stent graft (TAG, Gore) Gianturco Z-stent graft (Cook) covered with woven graft Stent graft (Talent, Medtronic) Tube stent graft (Talent, Medtronic) 2 Talent stent grafts
No No No No No No No Yes Yes No No No No No Yes No Yes Yes No
Yes No No No No No No Yes Yes No No No No Yes Yes No Yes Yes No
Yes No No Yes No No No No No Yes Yes Yes Yes Yes No No No No Yes
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Table I. Continued. Hemodynamic instability No Yes No No Yes No No No No Yes No No No Yes Yes Yes No No Yes Yes Yes Yes
Infection
Type of stent graft
Fistula occlusion
Adjunctive procedure
Lifelong antibiotics
No Yes Yes No No No No Yes No Yes No No No Yes Yes No No Yes No Yes No No
Gianturco Z-stent graft (Cook) covered with polyester tube Thoracic stent graft (Talent, Medtronic) Aortoiliac stent graft 2 Talent stent grafts AneuRx stent graft Talent stent graft Talent stent graft Thoracic stent graft (Excluder, Gore) 2 Talent stent grafts Aorto-uni-iliac stent graft Talent Dacron tube endograft Bifurcated stent graft (Excluder, Gore) Aorto-uni-iliac stent graft Talent Dacron tube endograft Talent Dacron tube endograft AneuRx stent graft (Medtronic) 2 Gianturco Z-stent grafts (Cook) AneuRx extender cuff (Medtronic) Z-stent (Cook) covered with PTFE (Impra) Bifurcated stent graft (Mintec, Stentor) Vanguard endovascular tube graft Palmaz stent graft covered with Dacron graft
No Yes No No Yes No No Yes No No No No No No No No No No No No No No
No Yes No No Yes No No Yes No Yes No No No No Yes No No No Yes No No No
No Yes Yes No No No No No No Yes Yes Yes Yes Yes Yes No No No Yes No Yes No
Complications Bleeding Persistent sepsis Sepsis, GI hemorrhage No No Sepsis Persistent sepsis No No Persistent sepsis Persistent sepsis, recurrent bleeding No Infection of R fem. interposition graft Postoperative fever Fluid collection/increased CRP No No Persistent sepsis Persistent sepsis No No Sepsis No No R ilio-femoral bypass, L CFA embolectomy Leakage, mediastinitis Mediastinal fluid collection No No Persistent sepsis No No Persistent sepsis, MOSF Persistent sepsis, ATN No Persistent sepsis No No
Follow-up 21 d 4d 4m 21 m 7m 18 m 12 m 8m 6m 3m 3m 6m 14 m 18 m 8m 20 m 13 m 2m 9d 36 m 14 m 3m 14 m 36 m 25 m 24 m 6m 18 m 13 m 34 m 23 m 26 d 11 m 33 m 8m 18 m 4.5 m
Mortality
Reason of death
Persistent/ recurrent/new infection
Recurrent bleeding
25 d NA NA NA NA NA NA NA NA 3m 3m NA NA NA NA NA NA 2m 9d NA NA NA 14 m NA NA 25 m NA NA 18 m 13 m NA NA 26 d 11 m NA NA NA 4.5 m
MOSF NA NA NA NA NA NA NA NA Sepsis Sepsis, recurrent bleeding NA NA NA NA NA NA Aortic rupture Aortic rupture NA NA NA MI Carcinoma NA Sepsis NA NA CVA MI NA NA MOSF MI NA NA NA Pneumonia
Yes Yes Yes No No Yes Yes No No Yes Yes No No No Yes No No Yes Yes No No Yes No No No Yes Yes No Yes No No No Yes Yes No Yes No No
Yes No Yes No No No No No No No Yes No No No No No No Yes Yes No No No No No No No No No No No No No No No No No No No
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Table I. Continued. Complications Recurrent fistula No No
Follow-up
Mortality
Reason of death
Persistent/ recurrent/new infection
Recurrent bleeding
5m 6m 13 m
NA NA NA
NA NA NA
Yes No No
Yes No No
M, male; F, female; P, primary; S, secondary; AEF, aorto-enteric fistula AA, abdominal aorta; TA, thoracic aorta; AEF, aortoenteric fistula; AAA, abdominal aortic aneurysm; d, day; m, month; MOSF, multiple organ system failure; CVA, cerebrovascular accident; MI, myocardial infarction; R, right; L, left; CFA, common femoral artery; NA, not applicable; NR, not reported.
aorto-jejunal fistula, aorto-esophageal fistula, AND endovascular or stent were used to extract the relevant abstracts. The references of the retrieved articles were also manually searched for any additional relevant articles. The literature search; study selection; and data extraction from the relevant studies were performed by two independent authors (G.A.A.; S.A.A.). Eligibility studies, data abstraction, and definitions of parameters and outcome endpoints. Studies considered for inclusion fulfilled the following criteria: (1) to report on the primary management of AEF with endovascular stent graft techniques, (2) to report on the presenting symptoms of the AEF, and (3) to report on the outcome after endovascular treatment of the AEF. All studies reporting on communication between the gastrointestinal tract and arteries other than the aorta were excluded. Data abstracted and parameters considered for further analysis were the following: patient age and gender, primary or secondary AEF, site of AEF, the cause of primary AEF, presence of hemodynamic instability, and signs and symptoms of infection preoperatively, type of stent graft used, fistula occlusion, adjunctive procedure, life-long antibiotics, complications, duration of follow-up, mortality, reason of death, persistent, recurrent, or new infection, and recurrent bleeding after treatment (Table I). Hemodynamic instability was considered if one or more of the following features were reported in the text of the articles: (1) systolic blood pressure less than 100 mm Hg plus tachycardia, (2) profound hypotension, (3) requirement of massive blood transfusion, and (4) massive hemorrhage. Clinical evidence of infection preoperatively was considered if any one of the following was reported: (1) fever, (2) white blood cell count more than 10,000/dL, (3) perigraft fluid or air on computed tomography (CT). If none of the above features was reported in the text, it was presumed that there was no hemodynamic instability or no clinical evidence of infection preoperatively. The endpoints of outcome were defined as either healed or treatment failure, depending on: (1) the presence or absence of documented signs and symptoms of recurrent, persistent, or new infection attributed to aortic stent graft and (2) the presence or absence of recurrent bleeding, up to the end of the follow-up period for each individual patient. Statistical analysis. We analyzed the data by using SPSS 15 for Windows (SPSS Inc, Chicago, Ill). The explor-
atory data analyses checked the distribution of values, and for each variable the proportion (percentage) of the total number of patients in the healed and persistent/recurrent/ new infection group was calculated. The 2 test was used to evaluate the differences between the healed and the persistent/ recurrent/new infection group for categorical variables. All statistical tests were two tailed, and a P value ⬍ .05 was considered statistically significant. The relationship between potential predictors and outcome was assessed using the odds ratio (ORs) and 95% confidence intervals (CI). The cumulative survival curve was calculated by using the Kaplan-Meier method. RESULTS Literature search results. Our search of the medical literature identified 42 studies, reporting on the endovascular stent graft repair of acute AEF, which were thoroughly reviewed. They were either case reports or small case series. Five studies were excluded due to inadequate individual patient data,7-11 one due to reporting on the endovascular management of an ilio-enteric fistula,12 and another three due to reporting on the secondary rather than primary endovascular management of AEF.13-15 Data were extracted from 33 reports that included 41 patients suffering from AEF, who were managed with endovascular stent graft repair, and were entered in the final analysis.16-48 Patient characteristics. The main characteristics of the patients are summarized in Table I. The study group consisted of 32 males and 9 females with a mean age of 68 years (range, 31-92 years), presenting with AEF primarily managed with endovascular stent graft placement. The mean follow-up period for these patients was 13 months (range, 0.13-36). Eighteen (43.90%) of the AEF were primary and 23 (56.10%) were secondary, the pathologic lesion was located in the abdominal aorta in 23 cases (56.10%) and in the thoracic aorta in 18 cases (43.90%). Of the 23 AEF located in the abdominal aorta only 5 (22%) were primary and 18 (78%) were secondary, whereas of the 18 AEF located in the thoracic aorta 13 (72%) were primary and only 5 (28%) were secondary. It was, therefore, found that thoracic aortic AEF were nine times more likely to be primary rather than secondary as compared with abdominal aortic AEF (P ⫽ .001; OR, 9.360; 95% CI, 2.239-39.121). The causes of primary AEF were aortic aneurysm-related in 6 cases (33%), gastrointestinal tract carcinoma-related in another 6 cases
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Table II. Analysis of potent predictors of persistent/recurrent/new infection after endovascular management of AEF Variable
Persistent/recurrent/new infection n ⫽ 18 (%)
Healed n ⫽ 23 (%)
P value
OR (95% CI)
Age ⬎70 years Male sex Primary/secondary AEF AA/TA Cancer Hemodynamic instability Signs of infection Fistula occlusion Adjunctive procedure Life-long antibiotics Post-op complications 30-day mortality
9 (50.00%) 16 (88.89%) 5/13 (27.78%/72.22%) 10/8 (55.56%/44.44%) 3 (16.67%) 9 (50.00%) 13 (72.22%) 3 (16.67%) 6 (33.33%) 8 (44.44%) 17 (94.44%) 3 (16.67%)
9 (39.13%) 16 (69.57%) 13/10 (56.52%/43.48%) 13/10 (56.52%/43.48%) 7 (30.43%) 13 (56.52%) 5 (21.74%) 5 (21.74%) 7 (30.43%) 10 (43.48%) 4 (17.39%) 0 (0.00%)
.486 .138 .066 .951 .308 .678 .001 .684 .843 .951 .000 .042
1.556 (0.447-5.413) 3.500 (0.628-19,496) 0.296 (0.079-1.108) 0.962 (0.278-3.331) 0.457 (0.099-2.101) 0.769 (0.223-2.654) 9.360 (2.239-39.121) 0.720 (0.147-3.520) 1.143 (0.305-4.289) 1.040 (0.300-3.603) 80.750 (8.203-794.944) 1.200 (0.976-1.475)
OR, odds ratio; CI, confidence interval; AEF, aortoenteric fistula; AA, abdominal aorta; TA, thoracic aorta.
(33%), trauma-related in 3 cases (17%), secondary to aortic ulcer in 1 case (6%), and secondary to an eroding duodenal stent in another case (6%) (Table I). Twenty-two of these patients (53.66%) had symptoms or signs of hemodynamic instability, as defined in the METHODS section, either on admission or during diagnostic workup, and were urgently transferred to the operating room. Clinical, laboratory, or imaging evidence of infection prior to surgical intervention, as defined in the METHODS section, was present in 43.90% of patients (18 patients). Imaging confirmation of the AEF was either endoscopic, with upper gastrointestinal endoscopy, or radiological, with angiography or CT, in all cases. The types of stent graft used for the endovascular repair of the AEF are shown in Table I. No conclusions on the associations between the type and configuration of the stent graft devises and the outcome can be drawn, because of the great variety of the stent grafts used at different anatomical sites. In 8 patients (19.51%) the endovascular management of the AEF was accompanied by repair of the contributing part of the gastrointestinal tract (fistula occlusion) with endoscopic, endovascular, or open surgical procedures; in one case a fibrin sealant was injected in the fistula tract endoscopically,34 in another case the fistula was catheterized under angiographic control and was injected with N-butyl 2-cyanocrylate,37 and in the remaining six cases the communication between the aorta and the bowel lumen was interrupted through a laparotomy or thoracotomy.23,24,29,31,32,39 Adjunctive procedures other than fistula occlusion included diverting iliostomy,41 CT-guided drainage of aortic sac,41 psoas abscess drainage,16 coilembolization of the aortic bifurcation,28 and balloon dilatation of the stent graft to treat leakage.45 Life-long antibiotic therapy postoperatively was reported to have been given to 18 patients (43.90%). Of interest is that of the 23 patients who were not presumed to have graft-related infection preoperatively, 7 patients (30%) were given life-long antibiotic therapy. During the follow-up period, 21 patients (51.22%) developed complications, the most serious of which were either related to recurrent/persistent/new
sepsis or recurrent bleeding (Table I). Twelve patients died during the follow-up period (29.27%), in 7 of whom (58.33%) this was due to septic complications. Factors associated with persistent/recurrent infection. The 41 patients were divided into two groups: one included those who did not develop symptoms or signs of graft-related infection or recurrent bleeding (healed group, n ⫽ 23), and the other included patients who developed graft-related infection or bleeding during the follow-up period (persistent/recurrent/new infection group, n ⫽ 18). The mean follow-up period for the healed and the recurrent/persistent/new infection group was 17 (range, 4.5-35) and 9 (range, 0.13-25) months, respectively. Various parameters which were suggested to be associated with the outcome after endovascular management of AEF were analyzed (Table II). Our analysis showed that of the 18 patients who presented with infection, 13 patients (72.22%) developed persistent or recurrent sepsis during the follow-up period and 5 patients (21.74%) healed. On the other hand, of the 23 patients who did not have evidence of infection preoperatively, 5 patients (21.74%) developed infection postoperatively and 18 patients (78.26%) healed. Univariate analysis found that signs of infection preoperatively and complications developed at any time after endovascular treatment of the AEF were factors associated with poor outcome (signs of infection preoperatively: P ⫽ .001; OR, 9.360; 95% CI, 2.239-39.121, complications: P ⬍ .0001; OR, 80.750; 95% CI, 8.203-794.944). Survival curves were plotted separately for the two groups of patients (Fig 1). The log-rank test was used to assess the difference in survival between the two groups, comparing events occurring at all time points on the survival curve. It was found that the healed group had a statistically significant difference in the survival times as compared with the persistent/recurrent/new infection group (P ⬍ .05). The standard error for estimated probability of 0.94 and 0.40 are 0.06 and 0.16, respectively, for the infection group. The standard error for estimated survival probability of 0.96 and 0.82 are 0.04 and 0.10, respectively, for the healed group.
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Survival Functions Outcome
1,0
Healed Infection Healed-censored Infectioncensored
Cum Survival
0,8
0,6
0,4
0,2
0,0 0,00
10,00
20,00
30,00
40,00
Months
Fig. Kaplan-Meier curves displaying the cumulative survival probability following endovascular treatment of aorto-enteric fistula (AEF), stratified by the presence or absence of persistent/recurrent/new infection.
DISCUSSION AEF represents one of the most uncommon but devastating clinical conditions a vascular surgeon may encounter. Despite progress in aortic surgery over the last decades, it is often a lethal condition, associated with dismal results. The physiological stress of massive hemorrhage along with that of sepsis, in the presence of co-morbid medical conditions, is magnified by a major operative procedure. The traditional management goals of AEF have been the control of hemorrhage, control of sepsis, and maintenance of lower limb perfusion. These are conventionally achieved with major reconstructive open surgery, which is accompanied with high morbidity and mortality rates.4-6 Endovascular techniques have emerged as another therapeutic option for the management of AEF achieving rapid control of bleeding with minimal insult, avoiding intervention in a hostile abdomen, and eliminating the complications associated with open surgical repair. However, it could be argued that only two of the three aforementioned fundamental management goals of AEF can be achieved with endovascular techniques, as the stent graft can effectively and rapidly control bleeding and maintain adequate distal perfusion, but the presence of aorto-enteric communication serves as a nidus for continuing bacterial growth and persistent infection. Therefore, placing a new prosthetic material in an already or potentially infected field, without eradicating the source of infection, creates concerns about the long-term safety and efficacy of the method. The first reports of successful endovascular treatment of AEF involving the abdominal and the thoracic aorta were performed a decade ago by Deshpande et al47 and Oliva et al,48 respectively, and were followed by several other reports with contradictory results. Our systematic review of the literature has found that persistent, recurrent, or new infection developed in 44% of the patients having under-
gone endovascular repair of the AEF, after a mean followup period of 13 months (range, 0.13-36). This figure most likely represents the lowest possible incidence of this complication, because unsuccessful outcomes with this approach would be less likely to be reported. It is slightly lower than the percentage found in the only case series identified in the literature, performed by Burks et al41 and Danneels et al,10 who reported a re-infection or AEF recurrence rate of 50% and 60%, respectively, for a mean follow-up period of 17 (range, 0.87-34) and 10 (range, 0.61-31), respectively. In the presence of such high treatment failure rates, our analysis attempted to identify whether there are any factors indicating poor outcome, which would possibly help find a subgroup of such patients in whom endovascular repair is not the best option. From the factors included in our analysis (Table II), it was found that gender and age (⬎70 years) do not affect the outcome. Furthermore, it was found that secondary as compared to primary AEF had an almost threefold increased risk of persistent/recurrent infection, though it did not reach statistical significance. This may be explained by the presence of a prosthetic material from the previous aortic reconstructive surgery, which remains in communication with the gut flora and acts as a nidus that perpetuates the infection. The site of the involved part of the gastrointestinal tract does not seem to affect the outcome, even though it could be expected that different types and concentrations of bacteria would have variable impact on the infectious process associated with the AEF. However, it was found that thoracic aortic as compared with abdominal aortic AEF were nine times more likely to be primary than secondary, which reached statistical significance (P ⫽ .001). This might be explained by the higher incidence of esophageal carcinoma invading the thoracic aorta than abdominal gastrointestinal carcinoma invading the aorta, the higher incidence of ingested foreign bodies eroding the esophagus than lower parts of the gastrointestinal tract, and the higher incidence of repaired abdominal aortic aneurysm than thoracic aortic aneurysm. In terms of the mode of presentation, our analysis found that the presence of hemodynamic instability preoperatively does not significantly influence outcome, whereas clinical, laboratory, or imaging signs of infection preoperatively were found as strong factors indicating poor outcome (P ⬍ .05). In the present analysis, the attempts to interrupt the communication between the aortic and bowel lumen with either minimally invasive (endoscopic or endovascular) or surgical methods did not achieve eradication of the source of infection (Table II), even though one report34 of endoscopic injection of fibrin sealant and another37 of intravascular occlusion of the fistula tract presented good shortterm results. Additionally, life-long antibiotic therapy did not achieve better outcome in the prevention of sepsis. Nevertheless, life-long antibiotics may still be useful, since the sicker patients with worse infections were probably maintained on antibiotics for longer periods than patients without signs of infection. The fact that 30% of patients who did not have evidence of infection preoperatively
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received life-long antibiotic therapy may be explained by the presumption by the respective authors that a foreign material was placed in a potentially infected field, communicating with the gastrointestinal tract. Our analysis has also shown that the persistent/recurrent/ new infection group developed a statistically significant higher complication rate (94.44% vs 17.29%; OR, 80.750; 95% CI, 8.203-794.944). Most complications were related to sepsis or recurrent bleeding developed in the period from the AEF repair up to the end of follow-up for each individual patient. Furthermore, survival analysis found that the persistent/recurrent infection group had statistically significant shorter 30-day and overall survival (Fig). As shown in Table I, most deaths were associated with septic or hemorrhagic complications of the AEF, which underscores the importance of the prevention of continuing contamination. The lack of uniform reporting results in difficulties to uniformly categorize the cases in respect to preoperative hemodynamic status, severity of bleeding and infection, as well as the length and type of antibiotic therapy. We attempted to set the definitions in order to proceed with the analysis of the various factors involved. Therefore, because of these weaknesses our results should be assessed with caution. In this systematic review, no comparison of the results after endovascular stent graft repair of AEF with those after conventional open surgical repair was undertaken. Because randomized multi-center studies comparing the outcome of endovascular with that of open repair in such an acute condition is difficult, a further systematic review to compare both methods would be an interesting undertaking. CONCLUSIONS Endovascular stent graft repair of AEF is associated with a high incidence of persistent/recurrent/new infection or recurrent bleeding. Our analysis has revealed that evidence of infection preoperatively is a factor associated with poor outcome after endovascular repair. Therefore, it appears that at least for this subgroup of patients, endovascular repair should be considered a bridge to more definitive repair at a later time, after the optimization of the patients’ condition. However, this requires further indication from other studies. We thank Elias Zintzaras, Associate Professor in the Department of Biomathematics at the University of Thessaly School of Medicine, Larissa, Greece, for his advice in the statistical interpretation of the results. AUTHOR CONTRIBUTIONS Conception and design: GA, ADG Analysis and interpretation: GA, AG, ML Data collection: GA, SA, SK, AG Writing the article: GA, SA Critical revision of the article: ML, AG Final approval of the article: GA, SK, SA, AG, ML, ADG Statistical analysis: GA, SK, AG
Obtained funding: Not applicable Overall responsibility: AG REFERENCES 1. Bergqvist D. Arterioenteric fistula. Review of a vascular emergency. Acta Chir Scand 1987;153:81-6. 2. Kuestner LM, Reilly LM, Jicha DL, Ehrenfeld WK, Goldstone J, Stoney RJ. Secondary aortoenteric fistula: contemporary outcome with use of extra-anatomic bypass and infected graft excision. J Vasc Surg 1995;21: 184-95. 3. Hallett JW Jr, Marshall DM, Petterson TM, Gray DT, Bower TC, Cherry KJ Jr, et al. Graft-related complications after abdominal aortic aneurysm repair: reassurance from a 36-year population-based experience. J Vasc Surg 1997;25:277-84. 4. Montgomery RS, Wilson SE. The surgical management of aortoenteric fistulas. Surg Clin North Am 1996;76:1147-57. 5. Busuttil SJ, Goldstone J. Diagnosis and management of aortoenteric fistulas. Semin Vasc Surg 2001;14:302-11. 6. Dorigo W, Pulli R, Azas L, Pratesi G, Innocenti AA, Pratesi C. Early and long-term results of conventional surgical treatment of secondary aortoenteric fistula. Eur J Vasc Endovasc Surg 2003;26:512-8. 7. Song Y, Liu Q, Shen H, Jia X, Zhang H, Qiao L. Diagnosis and management of primary aortoenteric fistulas– experience learned from 18 patients. Surgery 2008;143:43-50. 8. Baril DT, Carroccio A, Ellozy SH, Palchik E, Sachdev U, Jacobs TS, et al. Evolving strategies for the treatment of aortoenteric fistulas. J Vasc Surg 2006;44:250-7. 9. Haulon S, Koussa M, Beregi JP, Decoene C, Lions C, Warembourg H. Stent-graft repair of the thoracic aorta: short-term results. Ann Vasc Surg 2002;16:700-7. 10. Danneels MI, Verhagen HJ, Teijink JA, Cuypers P, Nevelsteen A, Vermassen FE. Endovascular repair for aorto-enteric fistula: a bridge too far or a bridge to surgery? Eur J Vasc Endovasc Surg 2006;32:27-33. 11. Bos WT, Verhoeven EL, Zeebregts CJ, Tielliu IF, Prins TR, Oranen BI, et al. Emergency endovascular stent grafting for thoracic aortic pathology. Vascular 2007;15:12-7. 12. Curti T, Freyrie A, Mirelli M, Rossi C, Paragona O, Resta F, et al. Endovascular treatment of an ilio-enteric fistula: a “bridge” to aortic homograft. Eur J Vasc Endovasc Surg 2000;20:204-6. 13. Eskandari MK, Makaroun MS, Abu-Elmagd KM, Billiar TR. Endovascular repair of an aortoduodenal fistula. J Endovasc Ther 2000;7:328-32. 14. Marone EM, Baccari P, Brioschi C, Tshomba Y, Staudacher C, Chiesa R. Surgical and endovascular treatment of secondary aortoesophageal fistula. J Thorac Cardiovasc Surg 2006;131:1409-10. 15. Yu CC, Lee WL, Ho WM, Wu CC, Liu TJ, P’eng FK. Successful management of latrogenic aortoduodenal fistula by intraaortic endovascular stent-graft and duodenal diversion. Hepatogastroenterology 2007;54:431-3. 16. Leonhardt H, Mellander S, Snygg J, Lönn L. Endovascular management of acute bleeding arterioenteric fistulas. Cardiovasc Intervent Radiol 2008 [Epub ahead of print]. 17. Taylor BJ, Stewart D, West P, Dunn JT, Cisek P. Endovascular repair of a secondary aortoesophageal fistula: a case report and review of the literature. Ann Vasc Surg 2007;21:167-71. 18. Chisci E, de Donato G, Setacci F, Stella A, Setacci C. Recurrent aortoenteric fistula: two different bridge solutions. Vascular 2007;15: 235-7. 19. Papacharalambous G, Skourtis G, Saliveros A, Karagannidis D, Makris S, Panousis P, et al. Endovascular treatment of a primary aortoduodenal fistula: 2-year follow-up of a case report. Vasc Endovascular Surg 2007;41:265-70. 20. Barleben AR, Baig MS, Kubaska SM, Fujitani RM, Gordon IA, Lane JS. Endovascular repair of an actively hemorrhaging aortoduodenal fistula. Ann Vasc Surg 2007;21:629-32. 21. Deshmukh H, Rathod K, Morani A, Garg A, Raut A. Percutaneous management of complications (aortoenteric fistula and sac abscess) following bypass surgery for abdominal aortic aneurysm. Cardiovasc Intervent Radiol 2007;30:778-81.
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22. Brountzos EN, Vasdekis S, Kostopanagiotou G, Danias N, Alexopoulou E, Petropoulou K, et al. Endovascular treatment of a bleeding secondary aorto-enteric fistula. A case report with 1-year follow-up. Cardiovasc Intervent Radiol 2007;30:1037-41. 23. Metz R, Kimmings AN, Verhagen HJ, Rinkes IH, van Hillegersberg R. Aortoesophageal fistula successfully treated by endovascular stent-graft. Ann Thorac Surg 2006;82:1117-9. 24. Ikeda Y, Morita N, Kurihara H, Niimi M, Okinaga K. A primary aortoesophageal fistula due to esophageal carcinoma successfully treated with endoluminal aortic stent grafting. J Thorac Cardiovasc Surg 2006;131:486-7. 25. Ting AC, Cheng SW, Ho P, Poon JT. Endovascular stent graft repair for infected thoracic aortic pseudoaneurysms–a durable option? J Vasc Surg 2006;44:701-5. 26. Verhey P, Best A, Lakin P, Nachiondo J, Petersen B. Successful endovascular treatment of aortoenteric fistula secondary to eroding duodenal stent. J Vasc Interv Radiol 2006;17:1345-8. 27. Shapiro M, Addis MD, Ellozy SH, Carroccio A, Teodorescu VJ, Marin ML. Successful endovascular treatment of bleeding aortoenteric fistula: a case report. Ann Vasc Surg 2006;20:817-9. 28. Kotsis T, Lioupis C, Tzanis A, Nasiopoulou P, Goumas K, Bakoyiannis K, et al. Endovascular repair of a bleeding secondary aortoenteric fistula with acute leg ischemia: a case report and review of the literature. J Vasc Interv Radiol 2006;17:563-7. 29. Biancari F, Romsi P, Perälä J, Koivukangas V, Cresti R, Juvonen T. Staged endovascular stent-grafting and surgical treatment of a secondary aortoduodenal fistula. Eur J Vasc Endovasc Surg 2006;31:42-3. 30. Suzuki S, Imoto K, Uchida K, Hashiyama N, Takanashi Y. Endovascular repair of a presumed aortoduodenal fistula. Ann Thorac Cardiovasc Surg 2005;11:424-8. 31. Assink J, Vierhout BP, Snellen JP, Benner PM, Paul MA, Cuesta MA, et al. Emergency endovascular repair of an aortoesophageal fistula caused by a foreign body. J Endovasc Ther 2005;12:129-33. 32. González-Fajardo JA, Gutiérrez V, Martín-Pedrosa M, Del Rio L, Carrera S, Vaquero C. Endovascular repair in the presence of aortic infection. Ann Vasc Surg 2005;19:94-8. 33. Nishibe T, Koizumi J, Kudo F, Miyazaki K, Nishibe M, Yasuda K. Successful endovascular stent-graft treatment for an aortoesophageal fistula caused by a descending thoracic aortic aneurysm: report of a case. Surg Today 2004;34:529-31. 34. Mok VW, Ting AC, Law S, Wong KH, Cheng SW, Wong J. Combined endovascular stent grafting and endoscopic injection of fibrin sealant for aortoenteric fistula complicating esophagectomy. J Vasc Surg 2004;40: 1234-7.
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35. Dieter RA Jr, Blum AS, Pozen TJ, Kuzycz G. Endovascular repair of aortojejunal fistula. Int Surg 2002;87:83-6. 36. Tomlinson MA, Gold B, Thomas MH, Browning NG. Endovascular stent graft repair of a recurrent aorto-enteric fistula. Eur J Vasc Endovasc Surg 2002;24:459-61. 37. Finch L, Heathcock RB, Quigley T, Jiranek G, Robinson D. Emergent treatment of a primary aortoenteric fistula with N-butyl 2-cyanoacrylate and endovascular stent. J Vasc Interv Radiol 2002;13:841-3. 38. Léobon B, Roux D, Mugniot A, Rousseau H, Cérene A, Glock Y, et al. Endovascular treatment of thoracic aortic fistulas. Ann Thorac Surg 2002;74:247-9. 39. Van Doorn RC, Reekers J, de Mol BA, Obertop H, Balm R. Aortoesophageal fistula secondary to mycotic thoracic aortic aneurysm: endovascular repair and transhiatal esophagectomy. J Endovasc Ther 2002; 9:212-7. 40. D’Ancona G, Dagenais F, Bauset R. Endoluminal stenting of the aorta as treatment of aortoesophageal fistula due to primary aortic disease. Tex Heart Inst J 2002;29:216-7. 41. Burks JA Jr, Faries PL, Gravereaux EC, Hollier LH, Marin ML. Endovascular repair of bleeding aortoenteric fistulas: a 5-year experience. J Vasc Surg 2001;34:1055-9. 42. Bond SE, McGuinness CL, Reidy JF, Taylor PR. Repair of secondary aortoesophageal fistula by endoluminal stent-grafting. J Endovasc Ther 2001;8:597-601. 43. Chuter TA, Lukaszewicz GC, Reilly LM, Kerlan RK, Faruqi R, Sawhney R, et al. Endovascular repair of a presumed aortoenteric fistula: late failure due to recurrent infection. J Endovasc Ther 2000;7:240-4. 44. Grabs AJ, Irvine CD, Lusby RJ. Stent-graft treatment for bleeding from a presumed aortoenteric fistula. J Endovasc Ther 2000;7:236-9. 45. Kato N, Tadanori H, Tanaka K, Yasuda F, Iwata M, Kawarada Y, et al. Aortoesophageal fistula-relief of massive hematemesis with an endovascular stent-graft. Eur J Radiol 2000;34:63-6. 46. Schlensak C, Doenst T, Spillner G, Blum U, Geiger A, Beyersdorf F. Palliative treatment of a secondary aortoduodenal fistula by stent-graft placement. Thorac Cardiovasc Surg 2000;48:41-2. 47. Deshpande A, Lovelock M, Mossop P, Denton M, Vidovich J, Gurry J. Endovascular repair of an aortoenteric fistula in a high-risk patient. J Endovasc Surg 1999;6:379-84. 48. Oliva VL, Bui BT, Leclerc G, Gravel D, Normandin D, Prenovault J, et al. Aortoesophageal fistula: repair with transluminal placement of a thoracic aortic stent-graft. J Vasc Interv Radiol 1997;8(1 Pt 1):35-8.
Submitted Jun 24, 2008; accepted Aug 26, 2008.
Outcome after endovascular stent graft repair of aortoenteric fistula: A systematic review George A. Antoniou, MD,a Stylianos Koutsias, MD,a Stavros A. Antoniou,a Andreas Georgiakakis, MD,a Miltos K. Lazarides, MD, EBSQvasc,b and Athanasios D. Giannoukas, MD, MSc, PhD, EBSQvasc,a Larissa and Alexandroupolis, Greece Background: Aortoenteric fistula (AEF) is a critical clinical condition, which may present with gastrointestinal hemorrhage, with or without signs of sepsis. Conventional open surgical repair is associated with high morbidity and mortality. Endovascular stent graft repair has been attempted, but recurrent infection remains of major concern. We conducted a systematic review to assess potential factors associated with poor outcome after endovascular treatment. Methods: The English literature was searched using the MEDLINE electronic database up to April 2008. All studies reporting on the primary management of primary or secondary AEF with endovascular stent graft repair were considered. Results: Data were extracted from 33 reports that included 41 patients and were entered in the final analysis. Persistent/recurrent/new infection or recurrent hemorrhage developed in 44% of the patients, after a mean follow-up period of 13 months (range, 0.13-36). Secondary, as compared to primary, AEF had an almost threefold increased risk of persistent/recurrent infection. Evidence of sepsis preoperatively was found to be a factor indicating unfavorable outcome (P < .05). Persistent/recurrent/new infection after treatment was associated with worse 30-day and overall survival compared with those who did not develop sepsis (P < .05). Conclusion: Endovascular stent graft repair of AEF was associated with a high incidence of infection or recurrent bleeding postoperatively. Evidence of sepsis preoperatively was indicating poor outcome. ( J Vasc Surg 2009;49:782-9.)
Aortoenteric fistula (AEF), defined as an abnormal communication between the aortic and bowel lumen, is a devastating clinical condition necessitating immediate surgical intervention. It can occur either in the setting of a primary process involving the aorta and the gastrointestinal tract or, more commonly, secondary to previous aortic reconstructive surgery. The condition may manifest with gastrointestinal hemorrhage alone or in combination with signs of sepsis. Despite its rarity, represented by an incidence in the range of 0.02 and 0.07% in autopsy studies for primary AEF and of less than 1% in patients after abdominal aortic reconstruction, AEF represents a significant clinical entity associated with high morbidity and mortality.1-3 Conventional surgical repair consists of extra-anatomic bypass grafting and aortic ligation for primary AEF, or in the case of secondary AEF, graft excision accomplished with extra-anatomic bypass or in situ aortic reconstruction. From the Department of Vascular Surgery, University Hospital of Larissa, Faculty of Medicine, University of Thessaly,a and the Department of Vascular Surgery, “Democritus” University of Thrace.b Competition of interest: none. Correspondence: Athanasios D. Giannoukas, MD, MSc, PhD, Associate Professor of Vascular Surgery, University of Thessaly Medical School, Chairman, Department of Vascular Surgery, University Hospital of Larissa, 41000 Larissa, Greece (e-mail: [email protected]). 0741-5214/$36.00 Copyright © 2009 by The Society for Vascular Surgery. doi:10.1016/j.jvs.2008.08.068
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These surgical procedures undertaken in a critically ill, severely exsanguinated and septic patient are associated with high operative morbidity and mortality rates.1,4-6 In view of these observations, less invasive endovascular aortic procedures, associated with less operative trauma and stress for the patient, have opened an alternative treatment option for this devastating complication. There are several studies reporting successful management of AEF with endovascular techniques (Table I) providing encouraging results. However, skepticism exists whether endovascular management of AEF should merely be a “bridge” to open surgery or may constitute a permanent solution, because it remains of serious concern the placement of a prosthetic material in an already infected field. We therefore conducted a systematic review of the literature and analyzed the reported cases to determine the factors associated with poor outcome and persistent infection after endovascular treatment of AEF. METHODS Search strategy. An electronic literature search of public domain databases (MEDLINE) was performed using a Web-based search engine (PubMed) for articles published between January 1990 and April 2008. The literature search was confined to studies published in English. The keywords aortoenteric fistula; aorto-duodenal fistula,
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Table I. Characteristics of patients Study
Year
Age
Gender
P/S
Site
Cause of primary AEF
Cancer
Leonhardt et al Taylor et al17 Chisci et al18 Papacharalambous et al19 Barleben et al20 Deshmukh et al21 Broutzos et al22 Metz et al23 Ikeda et al24 Ting et al25
2008 2007 2007 2007 2007 2007 2007 2006 2006 2006
Verhey et al26 Shapiro et al27 Kotsis et al28 Biancari et al29 Suzuki et al30 Assink et al31 Gonzalez-Fajardo et al32
2006 2006 2006 2006 2005 2005 2005
Nishibe et al33 Mok et al34 Dieter et al35 Tomlinson et al36 Finch et al37
2004 2004 2002 2002 2002
82 69 56 70 54 46 85 31 64 87 59 66 83 53 58 71 32 75 68 71 67 64 90 71
M F M M M M M M M M M F F M M M M M M F M M M F
S S S P P S S P P P P P S S S S P S P P P S S P
AA TA AA AA AA TA AA TA TA TA TA AA AA AA AA AA TA AA TA TA TA AA AA AA
No No No No No No No No Yes No Yes Yes No No No No No No No No Yes Yes No Yes
Leobon et al38
2002
van Doorn et al39 D’Ancona et al40 Burks et al41
2002 2002 2001
Bond et al42 Chuter et al43 Grabs et al44 Kato et al45 Schlensak et al46 Deshpande et al47 Oliva et al48
2001 2000 2000 2000 2000 1999 1997
61 80 66 78 73 82 92 73 76 88 58 76 67 59 64 67 40
M M F F M M M F M M F M M M M M M
S P P P S P S S S S S S S P S S P
TA TA TA TA AA AA AA AA TA AA TA AA AA TA AA AA TA
NA NA NA AAA Traumatic aortic dissection NA NA Aortic trauma due to ingestion of foreign body Aortic wall invasion by esophageal carcinoma NR Esophageal carcinoma-chemoirradiation Eroding duodenal stent NA NA NA NA Aortic trauma due to ingestion of foreign body NA Mycotic thoracic aortic aneurysm Thoracic aortic aneurysm Esophageal carcinoma-esophagectomy NA NA Metastatic ovarian carcinoma-peri-aortic adenopathy NA Thoracic aortic aneurysm Mycotic thoracic aortic aneurysm Aortic ulcer NA AAA NA NA NA NA NA NA NA Esophageal carcinoma-radiotherapy NA NA Esophageal carcinoma-esophagectomy
16
Hemodynamic instability Yes No No No Yes No Yes Yes Yes Yes No Yes Yes Yes No No Yes Yes Yes
No No Yes No No No No No No No No No No Yes No Yes Yes
Infection
Type of stent graft
Fistula occlusion
Adjunctive procedure
Lifelong antibiotics
Yes Yes Yes Yes No No No Yes No Yes Yes No Yes No Yes No No No Yes
Thoracic endoprosthesis (TAG, Gore) Straight sent graft with 1 extension Tube graft endoprosthesis (Talent, Medtronic) Bifurcated aortoiliac stent graft (Lifepath) 2 aortic extension cuffs (Excluder, Gore) Aortic stent graft (Zenith, Cook) Bifurcated stent graft (Excluder, Gore) Thoracic aortic stent graft (TAG, Gore) Gianturco Z-stent graft (Cook) covered with a Dacron graft AneuRx Zenith Aortic cuff (AneuRx, Medtronic) Bifurcated stent graft (Excluder, Gore) Aorto-uni-iliac stent graft (Zenith, Cook), F-F bypass Stent graft (TAG, Gore) Gianturco Z-stent graft (Cook) covered with woven graft Stent graft (Talent, Medtronic) Tube stent graft (Talent, Medtronic) 2 Talent stent grafts
No No No No No No No Yes Yes No No No No No Yes No Yes Yes No
Yes No No No No No No Yes Yes No No No No Yes Yes No Yes Yes No
Yes No No Yes No No No No No Yes Yes Yes Yes Yes No No No No Yes
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Table I. Continued. Hemodynamic instability No Yes No No Yes No No No No Yes No No No Yes Yes Yes No No Yes Yes Yes Yes
Infection
Type of stent graft
Fistula occlusion
Adjunctive procedure
Lifelong antibiotics
No Yes Yes No No No No Yes No Yes No No No Yes Yes No No Yes No Yes No No
Gianturco Z-stent graft (Cook) covered with polyester tube Thoracic stent graft (Talent, Medtronic) Aortoiliac stent graft 2 Talent stent grafts AneuRx stent graft Talent stent graft Talent stent graft Thoracic stent graft (Excluder, Gore) 2 Talent stent grafts Aorto-uni-iliac stent graft Talent Dacron tube endograft Bifurcated stent graft (Excluder, Gore) Aorto-uni-iliac stent graft Talent Dacron tube endograft Talent Dacron tube endograft AneuRx stent graft (Medtronic) 2 Gianturco Z-stent grafts (Cook) AneuRx extender cuff (Medtronic) Z-stent (Cook) covered with PTFE (Impra) Bifurcated stent graft (Mintec, Stentor) Vanguard endovascular tube graft Palmaz stent graft covered with Dacron graft
No Yes No No Yes No No Yes No No No No No No No No No No No No No No
No Yes No No Yes No No Yes No Yes No No No No Yes No No No Yes No No No
No Yes Yes No No No No No No Yes Yes Yes Yes Yes Yes No No No Yes No Yes No
Complications Bleeding Persistent sepsis Sepsis, GI hemorrhage No No Sepsis Persistent sepsis No No Persistent sepsis Persistent sepsis, recurrent bleeding No Infection of R fem. interposition graft Postoperative fever Fluid collection/increased CRP No No Persistent sepsis Persistent sepsis No No Sepsis No No R ilio-femoral bypass, L CFA embolectomy Leakage, mediastinitis Mediastinal fluid collection No No Persistent sepsis No No Persistent sepsis, MOSF Persistent sepsis, ATN No Persistent sepsis No No
Follow-up 21 d 4d 4m 21 m 7m 18 m 12 m 8m 6m 3m 3m 6m 14 m 18 m 8m 20 m 13 m 2m 9d 36 m 14 m 3m 14 m 36 m 25 m 24 m 6m 18 m 13 m 34 m 23 m 26 d 11 m 33 m 8m 18 m 4.5 m
Mortality
Reason of death
Persistent/ recurrent/new infection
Recurrent bleeding
25 d NA NA NA NA NA NA NA NA 3m 3m NA NA NA NA NA NA 2m 9d NA NA NA 14 m NA NA 25 m NA NA 18 m 13 m NA NA 26 d 11 m NA NA NA 4.5 m
MOSF NA NA NA NA NA NA NA NA Sepsis Sepsis, recurrent bleeding NA NA NA NA NA NA Aortic rupture Aortic rupture NA NA NA MI Carcinoma NA Sepsis NA NA CVA MI NA NA MOSF MI NA NA NA Pneumonia
Yes Yes Yes No No Yes Yes No No Yes Yes No No No Yes No No Yes Yes No No Yes No No No Yes Yes No Yes No No No Yes Yes No Yes No No
Yes No Yes No No No No No No No Yes No No No No No No Yes Yes No No No No No No No No No No No No No No No No No No No
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Table I. Continued. Complications Recurrent fistula No No
Follow-up
Mortality
Reason of death
Persistent/ recurrent/new infection
Recurrent bleeding
5m 6m 13 m
NA NA NA
NA NA NA
Yes No No
Yes No No
M, male; F, female; P, primary; S, secondary; AEF, aorto-enteric fistula AA, abdominal aorta; TA, thoracic aorta; AEF, aortoenteric fistula; AAA, abdominal aortic aneurysm; d, day; m, month; MOSF, multiple organ system failure; CVA, cerebrovascular accident; MI, myocardial infarction; R, right; L, left; CFA, common femoral artery; NA, not applicable; NR, not reported.
aorto-jejunal fistula, aorto-esophageal fistula, AND endovascular or stent were used to extract the relevant abstracts. The references of the retrieved articles were also manually searched for any additional relevant articles. The literature search; study selection; and data extraction from the relevant studies were performed by two independent authors (G.A.A.; S.A.A.). Eligibility studies, data abstraction, and definitions of parameters and outcome endpoints. Studies considered for inclusion fulfilled the following criteria: (1) to report on the primary management of AEF with endovascular stent graft techniques, (2) to report on the presenting symptoms of the AEF, and (3) to report on the outcome after endovascular treatment of the AEF. All studies reporting on communication between the gastrointestinal tract and arteries other than the aorta were excluded. Data abstracted and parameters considered for further analysis were the following: patient age and gender, primary or secondary AEF, site of AEF, the cause of primary AEF, presence of hemodynamic instability, and signs and symptoms of infection preoperatively, type of stent graft used, fistula occlusion, adjunctive procedure, life-long antibiotics, complications, duration of follow-up, mortality, reason of death, persistent, recurrent, or new infection, and recurrent bleeding after treatment (Table I). Hemodynamic instability was considered if one or more of the following features were reported in the text of the articles: (1) systolic blood pressure less than 100 mm Hg plus tachycardia, (2) profound hypotension, (3) requirement of massive blood transfusion, and (4) massive hemorrhage. Clinical evidence of infection preoperatively was considered if any one of the following was reported: (1) fever, (2) white blood cell count more than 10,000/dL, (3) perigraft fluid or air on computed tomography (CT). If none of the above features was reported in the text, it was presumed that there was no hemodynamic instability or no clinical evidence of infection preoperatively. The endpoints of outcome were defined as either healed or treatment failure, depending on: (1) the presence or absence of documented signs and symptoms of recurrent, persistent, or new infection attributed to aortic stent graft and (2) the presence or absence of recurrent bleeding, up to the end of the follow-up period for each individual patient. Statistical analysis. We analyzed the data by using SPSS 15 for Windows (SPSS Inc, Chicago, Ill). The explor-
atory data analyses checked the distribution of values, and for each variable the proportion (percentage) of the total number of patients in the healed and persistent/recurrent/ new infection group was calculated. The 2 test was used to evaluate the differences between the healed and the persistent/ recurrent/new infection group for categorical variables. All statistical tests were two tailed, and a P value ⬍ .05 was considered statistically significant. The relationship between potential predictors and outcome was assessed using the odds ratio (ORs) and 95% confidence intervals (CI). The cumulative survival curve was calculated by using the Kaplan-Meier method. RESULTS Literature search results. Our search of the medical literature identified 42 studies, reporting on the endovascular stent graft repair of acute AEF, which were thoroughly reviewed. They were either case reports or small case series. Five studies were excluded due to inadequate individual patient data,7-11 one due to reporting on the endovascular management of an ilio-enteric fistula,12 and another three due to reporting on the secondary rather than primary endovascular management of AEF.13-15 Data were extracted from 33 reports that included 41 patients suffering from AEF, who were managed with endovascular stent graft repair, and were entered in the final analysis.16-48 Patient characteristics. The main characteristics of the patients are summarized in Table I. The study group consisted of 32 males and 9 females with a mean age of 68 years (range, 31-92 years), presenting with AEF primarily managed with endovascular stent graft placement. The mean follow-up period for these patients was 13 months (range, 0.13-36). Eighteen (43.90%) of the AEF were primary and 23 (56.10%) were secondary, the pathologic lesion was located in the abdominal aorta in 23 cases (56.10%) and in the thoracic aorta in 18 cases (43.90%). Of the 23 AEF located in the abdominal aorta only 5 (22%) were primary and 18 (78%) were secondary, whereas of the 18 AEF located in the thoracic aorta 13 (72%) were primary and only 5 (28%) were secondary. It was, therefore, found that thoracic aortic AEF were nine times more likely to be primary rather than secondary as compared with abdominal aortic AEF (P ⫽ .001; OR, 9.360; 95% CI, 2.239-39.121). The causes of primary AEF were aortic aneurysm-related in 6 cases (33%), gastrointestinal tract carcinoma-related in another 6 cases
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Table II. Analysis of potent predictors of persistent/recurrent/new infection after endovascular management of AEF Variable
Persistent/recurrent/new infection n ⫽ 18 (%)
Healed n ⫽ 23 (%)
P value
OR (95% CI)
Age ⬎70 years Male sex Primary/secondary AEF AA/TA Cancer Hemodynamic instability Signs of infection Fistula occlusion Adjunctive procedure Life-long antibiotics Post-op complications 30-day mortality
9 (50.00%) 16 (88.89%) 5/13 (27.78%/72.22%) 10/8 (55.56%/44.44%) 3 (16.67%) 9 (50.00%) 13 (72.22%) 3 (16.67%) 6 (33.33%) 8 (44.44%) 17 (94.44%) 3 (16.67%)
9 (39.13%) 16 (69.57%) 13/10 (56.52%/43.48%) 13/10 (56.52%/43.48%) 7 (30.43%) 13 (56.52%) 5 (21.74%) 5 (21.74%) 7 (30.43%) 10 (43.48%) 4 (17.39%) 0 (0.00%)
.486 .138 .066 .951 .308 .678 .001 .684 .843 .951 .000 .042
1.556 (0.447-5.413) 3.500 (0.628-19,496) 0.296 (0.079-1.108) 0.962 (0.278-3.331) 0.457 (0.099-2.101) 0.769 (0.223-2.654) 9.360 (2.239-39.121) 0.720 (0.147-3.520) 1.143 (0.305-4.289) 1.040 (0.300-3.603) 80.750 (8.203-794.944) 1.200 (0.976-1.475)
OR, odds ratio; CI, confidence interval; AEF, aortoenteric fistula; AA, abdominal aorta; TA, thoracic aorta.
(33%), trauma-related in 3 cases (17%), secondary to aortic ulcer in 1 case (6%), and secondary to an eroding duodenal stent in another case (6%) (Table I). Twenty-two of these patients (53.66%) had symptoms or signs of hemodynamic instability, as defined in the METHODS section, either on admission or during diagnostic workup, and were urgently transferred to the operating room. Clinical, laboratory, or imaging evidence of infection prior to surgical intervention, as defined in the METHODS section, was present in 43.90% of patients (18 patients). Imaging confirmation of the AEF was either endoscopic, with upper gastrointestinal endoscopy, or radiological, with angiography or CT, in all cases. The types of stent graft used for the endovascular repair of the AEF are shown in Table I. No conclusions on the associations between the type and configuration of the stent graft devises and the outcome can be drawn, because of the great variety of the stent grafts used at different anatomical sites. In 8 patients (19.51%) the endovascular management of the AEF was accompanied by repair of the contributing part of the gastrointestinal tract (fistula occlusion) with endoscopic, endovascular, or open surgical procedures; in one case a fibrin sealant was injected in the fistula tract endoscopically,34 in another case the fistula was catheterized under angiographic control and was injected with N-butyl 2-cyanocrylate,37 and in the remaining six cases the communication between the aorta and the bowel lumen was interrupted through a laparotomy or thoracotomy.23,24,29,31,32,39 Adjunctive procedures other than fistula occlusion included diverting iliostomy,41 CT-guided drainage of aortic sac,41 psoas abscess drainage,16 coilembolization of the aortic bifurcation,28 and balloon dilatation of the stent graft to treat leakage.45 Life-long antibiotic therapy postoperatively was reported to have been given to 18 patients (43.90%). Of interest is that of the 23 patients who were not presumed to have graft-related infection preoperatively, 7 patients (30%) were given life-long antibiotic therapy. During the follow-up period, 21 patients (51.22%) developed complications, the most serious of which were either related to recurrent/persistent/new
sepsis or recurrent bleeding (Table I). Twelve patients died during the follow-up period (29.27%), in 7 of whom (58.33%) this was due to septic complications. Factors associated with persistent/recurrent infection. The 41 patients were divided into two groups: one included those who did not develop symptoms or signs of graft-related infection or recurrent bleeding (healed group, n ⫽ 23), and the other included patients who developed graft-related infection or bleeding during the follow-up period (persistent/recurrent/new infection group, n ⫽ 18). The mean follow-up period for the healed and the recurrent/persistent/new infection group was 17 (range, 4.5-35) and 9 (range, 0.13-25) months, respectively. Various parameters which were suggested to be associated with the outcome after endovascular management of AEF were analyzed (Table II). Our analysis showed that of the 18 patients who presented with infection, 13 patients (72.22%) developed persistent or recurrent sepsis during the follow-up period and 5 patients (21.74%) healed. On the other hand, of the 23 patients who did not have evidence of infection preoperatively, 5 patients (21.74%) developed infection postoperatively and 18 patients (78.26%) healed. Univariate analysis found that signs of infection preoperatively and complications developed at any time after endovascular treatment of the AEF were factors associated with poor outcome (signs of infection preoperatively: P ⫽ .001; OR, 9.360; 95% CI, 2.239-39.121, complications: P ⬍ .0001; OR, 80.750; 95% CI, 8.203-794.944). Survival curves were plotted separately for the two groups of patients (Fig 1). The log-rank test was used to assess the difference in survival between the two groups, comparing events occurring at all time points on the survival curve. It was found that the healed group had a statistically significant difference in the survival times as compared with the persistent/recurrent/new infection group (P ⬍ .05). The standard error for estimated probability of 0.94 and 0.40 are 0.06 and 0.16, respectively, for the infection group. The standard error for estimated survival probability of 0.96 and 0.82 are 0.04 and 0.10, respectively, for the healed group.
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Survival Functions Outcome
1,0
Healed Infection Healed-censored Infectioncensored
Cum Survival
0,8
0,6
0,4
0,2
0,0 0,00
10,00
20,00
30,00
40,00
Months
Fig. Kaplan-Meier curves displaying the cumulative survival probability following endovascular treatment of aorto-enteric fistula (AEF), stratified by the presence or absence of persistent/recurrent/new infection.
DISCUSSION AEF represents one of the most uncommon but devastating clinical conditions a vascular surgeon may encounter. Despite progress in aortic surgery over the last decades, it is often a lethal condition, associated with dismal results. The physiological stress of massive hemorrhage along with that of sepsis, in the presence of co-morbid medical conditions, is magnified by a major operative procedure. The traditional management goals of AEF have been the control of hemorrhage, control of sepsis, and maintenance of lower limb perfusion. These are conventionally achieved with major reconstructive open surgery, which is accompanied with high morbidity and mortality rates.4-6 Endovascular techniques have emerged as another therapeutic option for the management of AEF achieving rapid control of bleeding with minimal insult, avoiding intervention in a hostile abdomen, and eliminating the complications associated with open surgical repair. However, it could be argued that only two of the three aforementioned fundamental management goals of AEF can be achieved with endovascular techniques, as the stent graft can effectively and rapidly control bleeding and maintain adequate distal perfusion, but the presence of aorto-enteric communication serves as a nidus for continuing bacterial growth and persistent infection. Therefore, placing a new prosthetic material in an already or potentially infected field, without eradicating the source of infection, creates concerns about the long-term safety and efficacy of the method. The first reports of successful endovascular treatment of AEF involving the abdominal and the thoracic aorta were performed a decade ago by Deshpande et al47 and Oliva et al,48 respectively, and were followed by several other reports with contradictory results. Our systematic review of the literature has found that persistent, recurrent, or new infection developed in 44% of the patients having under-
gone endovascular repair of the AEF, after a mean followup period of 13 months (range, 0.13-36). This figure most likely represents the lowest possible incidence of this complication, because unsuccessful outcomes with this approach would be less likely to be reported. It is slightly lower than the percentage found in the only case series identified in the literature, performed by Burks et al41 and Danneels et al,10 who reported a re-infection or AEF recurrence rate of 50% and 60%, respectively, for a mean follow-up period of 17 (range, 0.87-34) and 10 (range, 0.61-31), respectively. In the presence of such high treatment failure rates, our analysis attempted to identify whether there are any factors indicating poor outcome, which would possibly help find a subgroup of such patients in whom endovascular repair is not the best option. From the factors included in our analysis (Table II), it was found that gender and age (⬎70 years) do not affect the outcome. Furthermore, it was found that secondary as compared to primary AEF had an almost threefold increased risk of persistent/recurrent infection, though it did not reach statistical significance. This may be explained by the presence of a prosthetic material from the previous aortic reconstructive surgery, which remains in communication with the gut flora and acts as a nidus that perpetuates the infection. The site of the involved part of the gastrointestinal tract does not seem to affect the outcome, even though it could be expected that different types and concentrations of bacteria would have variable impact on the infectious process associated with the AEF. However, it was found that thoracic aortic as compared with abdominal aortic AEF were nine times more likely to be primary than secondary, which reached statistical significance (P ⫽ .001). This might be explained by the higher incidence of esophageal carcinoma invading the thoracic aorta than abdominal gastrointestinal carcinoma invading the aorta, the higher incidence of ingested foreign bodies eroding the esophagus than lower parts of the gastrointestinal tract, and the higher incidence of repaired abdominal aortic aneurysm than thoracic aortic aneurysm. In terms of the mode of presentation, our analysis found that the presence of hemodynamic instability preoperatively does not significantly influence outcome, whereas clinical, laboratory, or imaging signs of infection preoperatively were found as strong factors indicating poor outcome (P ⬍ .05). In the present analysis, the attempts to interrupt the communication between the aortic and bowel lumen with either minimally invasive (endoscopic or endovascular) or surgical methods did not achieve eradication of the source of infection (Table II), even though one report34 of endoscopic injection of fibrin sealant and another37 of intravascular occlusion of the fistula tract presented good shortterm results. Additionally, life-long antibiotic therapy did not achieve better outcome in the prevention of sepsis. Nevertheless, life-long antibiotics may still be useful, since the sicker patients with worse infections were probably maintained on antibiotics for longer periods than patients without signs of infection. The fact that 30% of patients who did not have evidence of infection preoperatively
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received life-long antibiotic therapy may be explained by the presumption by the respective authors that a foreign material was placed in a potentially infected field, communicating with the gastrointestinal tract. Our analysis has also shown that the persistent/recurrent/ new infection group developed a statistically significant higher complication rate (94.44% vs 17.29%; OR, 80.750; 95% CI, 8.203-794.944). Most complications were related to sepsis or recurrent bleeding developed in the period from the AEF repair up to the end of follow-up for each individual patient. Furthermore, survival analysis found that the persistent/recurrent infection group had statistically significant shorter 30-day and overall survival (Fig). As shown in Table I, most deaths were associated with septic or hemorrhagic complications of the AEF, which underscores the importance of the prevention of continuing contamination. The lack of uniform reporting results in difficulties to uniformly categorize the cases in respect to preoperative hemodynamic status, severity of bleeding and infection, as well as the length and type of antibiotic therapy. We attempted to set the definitions in order to proceed with the analysis of the various factors involved. Therefore, because of these weaknesses our results should be assessed with caution. In this systematic review, no comparison of the results after endovascular stent graft repair of AEF with those after conventional open surgical repair was undertaken. Because randomized multi-center studies comparing the outcome of endovascular with that of open repair in such an acute condition is difficult, a further systematic review to compare both methods would be an interesting undertaking. CONCLUSIONS Endovascular stent graft repair of AEF is associated with a high incidence of persistent/recurrent/new infection or recurrent bleeding. Our analysis has revealed that evidence of infection preoperatively is a factor associated with poor outcome after endovascular repair. Therefore, it appears that at least for this subgroup of patients, endovascular repair should be considered a bridge to more definitive repair at a later time, after the optimization of the patients’ condition. However, this requires further indication from other studies. We thank Elias Zintzaras, Associate Professor in the Department of Biomathematics at the University of Thessaly School of Medicine, Larissa, Greece, for his advice in the statistical interpretation of the results. AUTHOR CONTRIBUTIONS Conception and design: GA, ADG Analysis and interpretation: GA, AG, ML Data collection: GA, SA, SK, AG Writing the article: GA, SA Critical revision of the article: ML, AG Final approval of the article: GA, SK, SA, AG, ML, ADG Statistical analysis: GA, SK, AG
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Submitted Jun 24, 2008; accepted Aug 26, 2008.